Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T00:58:41.089Z Has data issue: false hasContentIssue false

Cognitive control of attention is differentially affected in trauma-exposed individuals with and without post-traumatic stress disorder

Published online by Cambridge University Press:  09 May 2012

K. S. Blair*
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
M. Vythilingam
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
S. L. Crowe
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
D. E. McCaffrey
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
P. Ng
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
C. C. Wu
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
M. Scaramozza
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
K. Mondillo
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
D. S. Pine
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
D. S. Charney
Affiliation:
Mount Sinai School of Medicine, New York, NY, USA
R. J. R. Blair
Affiliation:
National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
*
*Address for correspondence: K. S. Blair, Ph.D., National Institute of Mental Health, 15K North Drive, MSC 2670, Bethesda, MD 20892, USA. (Email: [email protected])

Abstract

Background

This study aimed to determine whether patients with post-traumatic stress disorder (PTSD) show difficulty in recruitment of the regions of the frontal and parietal cortex implicated in top-down attentional control in the presence and absence of emotional distracters.

Method

Unmedicated individuals with PTSD (n = 14), and age-, IQ- and gender-matched individuals exposed to trauma (n = 15) and healthy controls (n = 19) were tested on the affective number Stroop task. In addition, blood oxygen level-dependent responses, as measured via functional magnetic resonance imaging, were recorded.

Results

Patients with PTSD showed disrupted recruitment of lateral regions of the superior and inferior frontal cortex as well as the parietal cortex in the presence of negative distracters. Trauma-comparison individuals showed indications of a heightened ability to recruit fronto-parietal regions implicated in top-down attentional control across distracter conditions.

Conclusions

These results are consistent with suggestions that emotional responsiveness can interfere with the recruitment of regions implicated in top-down attentional control; the heightened emotional responding of patients with PTSD may lead to the heightened interference in the recruitment of these regions.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Armony, JL, Corbo, V, Clement, MH, Brunet, A (2005). Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expressions. American Journal of Psychiatry 162, 19611963.CrossRefGoogle ScholarPubMed
Bar-Haim, Y, Lamy, D, Pergamin, L, Bakermans-Kranenburg, MJ, van IJzendoorn, MH (2007). Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychological Bulletin 133, 124.CrossRefGoogle ScholarPubMed
Bishop, SJ (2008). Trait anxiety and impoverished prefrontal control of attention. Nature Neuroscience 12, 9298.CrossRefGoogle ScholarPubMed
Blair, KS, Smith, BW, Mitchell, DG, Morton, J, Vythilingam, M, Pessoa, L, Fridberg, D, Zametkin, A, Sturman, D, Nelson, EE, Drevets, WC, Pine, DS, Martin, A, Blair, RJ (2007). Modulation of emotion by cognition and cognition by emotion. Neuroimage 35, 430440.CrossRefGoogle ScholarPubMed
Blake, DD, Weathers, FW, Nagy, LM, Kaloupek, DG, Gusman, FD, Charney, DS, Keane, TM (1995). The development of a clinician-administered PTSD scale. Journal of Traumatic Stress 8, 7590.Google ScholarPubMed
Blake, DD, Weathers, FW, Nagy, LM, Kaloupek, DG, Kiaumnizer, G, Charney, DS (1990). A clinician rating scale for assessing current and lifetime PTSD: the CAPS-1. Behavior Therapist 13, 187188.Google Scholar
Bremner, JD, Vermetten, E, Vythilingam, M, Afzal, N, Schmahl, C, Elzinga, B, Charney, DS (2004). Neural correlates of the classic color and emotional Stroop in women with abuse-related posttraumatic stress disorder. Biologial Psychiatry 55, 612620.CrossRefGoogle ScholarPubMed
Britton, JC, Phan, KL, Taylor, SF, Fig, LM, Liberzon, I (2005). Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry 57, 832840.CrossRefGoogle ScholarPubMed
Bryant, RA, Harvey, AG (1995). Processing threatening information in posttraumatic stress disorder. Journal of Abnormal Psychology 104, 537541.CrossRefGoogle ScholarPubMed
Buckley, TC, Blanchard, EB, Neill, WT (2000). Information processing and PTSD: a review of the empirical literature. Clinical Psychology Review 20, 10411065.CrossRefGoogle ScholarPubMed
Coles, ME, Heimberg, RG (2002). Memory biases in the anxiety disorders: current status. Clinical Psychology Review 22, 587627.CrossRefGoogle ScholarPubMed
Daniels, JK, McFarlane, AC, Bluhm, RL, Moores, KA, Clark, CR, Shaw, ME, Williamson, PC, Densmore, M, Lanius, RA (2010). Switching between executive and default mode networks in posttraumatic stress disorder: alterations in functional connectivity. Journal of Psychiatry and Neuroscience 35, 258266.CrossRefGoogle ScholarPubMed
Desimone, R, Duncan, J (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience 18, 193222.CrossRefGoogle ScholarPubMed
El Khoury-Malhame, M, Reynaud, E, Soriano, A, Michael, K, Salgado-Pineda, P, Zendjidjian, X, Gellato, C, Eric, F, Lefebvre, MN, Rouby, F, Samuelian, JC, Anton, JL, Blin, O, Khalfa, S (2011). Amygdala activity correlates with attentional bias in PTSD. Neuropsychologia 49, 19691973.CrossRefGoogle ScholarPubMed
Felmingham, K, Williams, LM, Kemp, AH, Liddell, B, Falconer, E, Peduto, A, Bryant, R (2010). Neural responses to masked fear faces: sex differences and trauma exposure in posttraumatic stress disorder. Journal of Abnormal Psychology 119, 241247.CrossRefGoogle ScholarPubMed
First, M, Spitzer, R, Gibbon, M, Williams, J (1997). Structured Clinical Interview for DSM-IV. American Psychiatric Press: Washington, DC.Google Scholar
Foa, EB, Feske, U, Murdock, TB, Kozak, MJ, McCarthy, PR (1991). Processing of threat-related information in rape victims. Journal of Abnormal Psychology 100, 156162.CrossRefGoogle ScholarPubMed
Holman, EA, Silver, RC, Waitzkin, H (2000). Traumatic life events in primary care patients: a study in an ethnically diverse sample. Archives of Family Medicine 9, 802810.CrossRefGoogle Scholar
Jatzko, A, Schmitt, A, Demirakca, T, Weimer, E, Braus, DF (2006). Disturbance in the neural circuitry underlying positive emotional processing in post-traumatic stress disorder (PTSD). An fMRI study. European Archives of Psychiatry and Clinical Neuroscience 256, 112114.CrossRefGoogle ScholarPubMed
Kastner, S, Ungerleider, LG (2000). Mechanisms of visual attention in the human cortex. Annual Review of Neuroscience 23, 315341.Google ScholarPubMed
Kim, M, Chey, J, Chung, A, Bae, S, Khang, H, Ham, B, Yoon, S, Jeong, D, Lyoo, K (2008). Diminished rostral anterior cingulate activity in response to threat-related events in posttraumatic stress disorder. Journal of Psychiatry Research 42, 268277.CrossRefGoogle ScholarPubMed
Lang, PJ, Greenwald, MK (1988). The International Affective Picture System Standardization Procedure and Initial Group Results for Affective Judgements: Technical Reports 1A & 1B. Center for Research in Psychophysiology, University of Florida: Gainesville.Google Scholar
McNally, RJ, Kaspi, SP, Riemann, BC, Zeitlin, SB (1990). Selective processing of threat cues in posttraumatic stress disorder. Journal of Abnormal Psychology 99, 398402.CrossRefGoogle ScholarPubMed
Mitchell, DG, Nakic, M, Fridberg, D, Kamel, N, Pine, DS, Blair, RJ (2007). The impact of processing load on emotion. Neuroimage 34, 12991309.CrossRefGoogle ScholarPubMed
Moores, KA, Clark, CR, McFarlane, AC, Brown, GC, Puce, A, Taylor, DJ (2008). Abnormal recruitment of working memory updating networks during maintenance of trauma-neutral information in post-traumatic stress disorder. Psychiatry Research 163, 156170.CrossRefGoogle ScholarPubMed
Morey, RA, Petty, CM, Cooper, DA, Labar, KS, McCarthy, G (2008). Neural systems for executive and emotional processing are modulated by symptoms of posttraumatic stress disorder in Iraq War veterans. Psychiatry Research: Neuroimaging 162, 5972.CrossRefGoogle ScholarPubMed
New, AS, Hazlett, EA, Newmark, RE, Zhang, J, Triebwasser, J, Meyerson, D, Lazarus, S, Trisdorfer, R, Goldstein, KE, Goodman, M, Koenigsberg, HW, Flory, JD, Siever, LJ, Buchsbaum, MS (2009). Laboratory induced aggression: a positron emission tomography study of aggressive individuals with borderline personality disorder. Biological Psychiatry 66, 11071114.CrossRefGoogle ScholarPubMed
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JD (2002). Rethinking feelings: an FMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience 14, 12151229.CrossRefGoogle ScholarPubMed
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242249.CrossRefGoogle ScholarPubMed
Pannu Hayes, J, Labar, KS, Petty, CM, McCarthy, G, Morey, RA (2009). Alterations in the neural circuitry for emotion and attention associated with posttraumatic stress symptomatology. Psychiatry Research 172, 715.CrossRefGoogle ScholarPubMed
Pessoa, L (2009). How do emotion and motivation direct executive control? Trends in Cognitive Science 13, 160166.CrossRefGoogle ScholarPubMed
Pessoa, L, McKenna, M, Gutierrez, E, Ungerleider, LG (2002). Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences USA 99, 1145811463.CrossRefGoogle ScholarPubMed
Pessoa, L, Padmala, S, Morland, T (2005). Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation. Neuroimage 28, 249255.CrossRefGoogle ScholarPubMed
Rauch, SL, Shin, LM, Phelps, EA (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research – past, present, and future. Biological Psychiatry 60, 376382.CrossRefGoogle ScholarPubMed
Rauch, SL, Whalen, PJ, Shin, LM, McInerney, SC, Macklin, ML, Lasko, NB, Orr, SP, Pitman, RK (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry 47, 769776.CrossRefGoogle ScholarPubMed
Rush, AJ, Giles, DE, Schlesser, MA, Fulton, CL, Weissenburger, J, Burns, C (1986). The Inventory for Depressive Symptomatology (IDS): preliminary findings. Psychiatry Research 18, 6587.CrossRefGoogle ScholarPubMed
Sailer, U, Robinson, S, Fischmeister, FP, Konig, D, Oppenauer, C, Lueger-Schuster, B, Moser, E, Kryspin-Exner, I, Bauer, H (2008). Altered reward processing in the nucleus accumbens and mesial prefrontal cortex of patients with posttraumatic stress disorder. Neuropsychologia 46, 28362844.CrossRefGoogle ScholarPubMed
Shear, MK, Vander Bilt, J, Rucci, P, Endicott, J, Lydiard, B, Otto, NW, Pollack, MH, Chandler, L, Williams, J, Ali, A, Frank, DM (2001). Reliability and validity of a structured interview guide for the Hamilton Anxiety Rating Scale (SIGH-A). Depression and Anxiety 13, 166178.CrossRefGoogle ScholarPubMed
Shin, LM, Liberzon, I (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35, 169191.CrossRefGoogle ScholarPubMed
Shin, LM, Whalen, PJ, Pitman, RK, Bush, G, Macklin, ML, Lasko, NB, Orr, SP, McInerney, SC, Rauch, SL (2001). An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biological Psychiatry 50, 932942.CrossRefGoogle ScholarPubMed
Shin, LM, Wright, CI, Cannistraro, PA, Wedig, MM, McMullin, K, Martis, B, Macklin, ML, Lasko, NB, Cavanagh, SR, Krangel, TS, Orr, SP, Pitman, RK, Whalen, PJ, Rauch, SL (2005). A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Archives of General Psychiatry 62, 273281.CrossRefGoogle ScholarPubMed
Talairach, J, Tournoux, P (1988). Co-planar Stereotaxic Atlas of the Human Brain. Thieme: New York, NY.Google Scholar
Vythilingam, M, Blair, KS, McCaffrey, D, Scaramozza, M, Jones, M, Nakic, M, Mondillo, K, Hadd, K, Bonne, O, Mitchell, DG, Pine, DS, Charney, DS, Blair, RJ (2007). Biased emotional attention in post-traumatic stress disorder: a help as well as a hindrance? Psychological Medicine 37, 14451455.CrossRefGoogle ScholarPubMed
Williams, JM, Mathews, A, MacLeod, C (1996). The emotional Stroop task and psychopathology. Psychological Bulletin 120, 324.CrossRefGoogle ScholarPubMed
Wolf, EJ, Miller, MW, McKinney, AE (2009). Emotional processing in PTSD: heightened negative emotionality to unpleasant photographic stimuli. Journal of Nervous and Mental Disease 197, 419426.CrossRefGoogle ScholarPubMed